Abstract
Thermococcus gammatolerans, the most radioresistant archaeon known to date, is an anaerobic and hyperthermophilic sulfur-reducing organism living in deep-sea hydrothermal vents. Knowledge of mechanisms underlying archaeal metal tolerance in such metal-rich ecosystem is still poorly documented. We showed that T. gammatolerans exhibits high resistance to cadmium (Cd), cobalt (Co) and zinc (Zn), a weaker tolerance to nickel (Ni), copper (Cu) and arsenate (AsO4) and that cells exposed to 1 mM Cd exhibit a cellular Cd concentration of 67 µM. A time-dependent transcriptomic analysis using microarrays was performed at a non-toxic (100 µM) and a toxic (1 mM) Cd dose. The reliability of microarray data was strengthened by real time RT-PCR validations. Altogether, 114 Cd responsive genes were revealed and a substantial subset of genes is related to metal homeostasis, drug detoxification, re-oxidization of cofactors and ATP production. This first genome-wide expression profiling study of archaeal cells challenged with Cd showed that T. gammatolerans withstands induced stress through pathways observed in both prokaryotes and eukaryotes but also through new and original strategies. T. gammatolerans cells challenged with 1 mM Cd basically promote: 1) the induction of several transporter/permease encoding genes, probably to detoxify the cell; 2) the upregulation of Fe transporters encoding genes to likely compensate Cd damages in iron-containing proteins; 3) the induction of membrane-bound hydrogenase (Mbh) and membrane-bound hydrogenlyase (Mhy2) subunits encoding genes involved in recycling reduced cofactors and/or in proton translocation for energy production. By contrast to other organisms, redox homeostasis genes appear constitutively expressed and only a few genes encoding DNA repair proteins are regulated. We compared the expression of 27 Cd responsive genes in other stress conditions (Zn, Ni, heat shock, γ-rays), and showed that the Cd transcriptional pattern is comparable to other metal stress transcriptional responses (Cd, Zn, Ni) but not to a general stress response.
Highlights
While trace amounts of several metals such as iron (Fe), manganese (Mn), copper (Cu), nickel (Ni), cobalt (Co) and zinc (Zn) are essential to support cell growth, elevated amounts induce cell toxicity [1]
Cell growth was scored at 24 hrs and at 48 hrs to check that cells did not need more time to recover, but no difference was observed at a metal concentration that completely inhibits cell growth (MIC)
Our large-scale proteomic analysis showed that most of them were expressed when cells grew in a rich proteinous medium containing Su [25], and we showed here that, among the dozen of T. gammatolerans Feast/famine Regulatory Proteins (FFRPs) regulators, the 3 halves FFRPs displayed the same behavior under metal stress condition
Summary
While trace amounts of several metals such as iron (Fe), manganese (Mn), copper (Cu), nickel (Ni), cobalt (Co) and zinc (Zn) are essential to support cell growth, elevated amounts induce cell toxicity [1]. Other non-essential metals, such as cadmium (Cd), cause severe toxicity even at very low concentrations (reviewed in [2]). Cd induces several cellular dysfunctions and enhances mutagenesis and cell death. Cd ions can displace cognate metals leading to enzymatic inactivation and induce toxicity [3]. Microbes have evolved to efficiently adjust cellular homeostasis by regulating metal import, and in the case of a massive exposure, activate efflux pumps [4]. The complexes are sequestered into a limited area to prevent the free circulation of metal ions in the cytosol
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